Human leg model predicts ankle muscle-tendon morphology, state, roles and energetics in walking
A common feature in biological neuromuscular systems is the redundancy in joint actuation. Understanding how these redundancies are resolved in typical joint movements has been a long-standing problem in biomechanics, neuroscience and prosthetics. Many empirical studies have uncovered neural, mechan...
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Published in | PLoS computational biology Vol. 7; no. 3; p. e1001107 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
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01.03.2011
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Abstract | A common feature in biological neuromuscular systems is the redundancy in joint actuation. Understanding how these redundancies are resolved in typical joint movements has been a long-standing problem in biomechanics, neuroscience and prosthetics. Many empirical studies have uncovered neural, mechanical and energetic aspects of how humans resolve these degrees of freedom to actuate leg joints for common tasks like walking. However, a unifying theoretical framework that explains the many independent empirical observations and predicts individual muscle and tendon contributions to joint actuation is yet to be established. Here we develop a computational framework to address how the ankle joint actuation problem is resolved by the neuromuscular system in walking. Our framework is founded upon the proposal that a consideration of both neural control and leg muscle-tendon morphology is critical to obtain predictive, mechanistic insight into individual muscle and tendon contributions to joint actuation. We examine kinetic, kinematic and electromyographic data from healthy walking subjects to find that human leg muscle-tendon morphology and neural activations enable a metabolically optimal realization of biological ankle mechanics in walking. This optimal realization (a) corresponds to independent empirical observations of operation and performance of the soleus and gastrocnemius muscles, (b) gives rise to an efficient load-sharing amongst ankle muscle-tendon units and (c) causes soleus and gastrocnemius muscle fibers to take on distinct mechanical roles of force generation and power production at the end of stance phase in walking. The framework outlined here suggests that the dynamical interplay between leg structure and neural control may be key to the high walking economy of humans, and has implications as a means to obtain insight into empirically inaccessible features of individual muscle and tendons in biomechanical tasks. |
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AbstractList | A common feature in biological neuromuscular systems is the redundancy in joint actuation. Understanding how these redundancies are resolved in typical joint movements has been a long-standing problem in biomechanics, neuroscience and prosthetics. Many empirical studies have uncovered neural, mechanical and energetic aspects of how humans resolve these degrees of freedom to actuate leg joints for common tasks like walking. However, a unifying theoretical framework that explains the many independent empirical observations and predicts individual muscle and tendon contributions to joint actuation is yet to be established. Here we develop a computational framework to address how the ankle joint actuation problem is resolved by the neuromuscular system in walking. Our framework is founded upon the proposal that a consideration of both neural control and leg muscle-tendon morphology is critical to obtain predictive, mechanistic insight into individual muscle and tendon contributions to joint actuation. We examine kinetic, kinematic and electromyographic data from healthy walking subjects to find that human leg muscle-tendon morphology and neural activations enable a metabolically optimal realization of biological ankle mechanics in walking. This optimal realization (a) corresponds to independent empirical observations of operation and performance of the soleus and gastrocnemius muscles, (b) gives rise to an efficient load-sharing amongst ankle muscle-tendon units and (c) causes soleus and gastrocnemius muscle fibers to take on distinct mechanical roles of force generation and power production at the end of stance phase in walking. The framework outlined here suggests that the dynamical interplay between leg structure and neural control may be key to the high walking economy of humans, and has implications as a means to obtain insight into empirically inaccessible features of individual muscle and tendons in biomechanical tasks. A common feature in biological neuromuscular systems is the redundancy in joint actuation. Understanding how these redundancies are resolved in typical joint movements has been a long-standing problem in biomechanics, neuroscience and prosthetics. Many empirical studies have uncovered neural, mechanical and energetic aspects of how humans resolve these degrees of freedom to actuate leg joints for common tasks like walking. However, a unifying theoretical framework that explains the many independent empirical observations and predicts individual muscle and tendon contributions to joint actuation is yet to be established. Here we develop a computational framework to address how the ankle joint actuation problem is resolved by the neuromuscular system in walking. Our framework is founded upon the proposal that a consideration of both neural control and leg muscle-tendon morphology is critical to obtain predictive, mechanistic insight into individual muscle and tendon contributions to joint actuation. We examine kinetic, kinematic and electromyographic data from healthy walking subjects to find that human leg muscle-tendon morphology and neural activations enable a metabolically optimal realization of biological ankle mechanics in walking. This optimal realization (a) corresponds to independent empirical observations of operation and performance of the soleus and gastrocnemius muscles, (b) gives rise to an efficient load-sharing amongst ankle muscle-tendon units and (c) causes soleus and gastrocnemius muscle fibers to take on distinct mechanical roles of force generation and power production at the end of stance phase in walking. The framework outlined here suggests that the dynamical interplay between leg structure and neural control may be key to the high walking economy of humans, and has implications as a means to obtain insight into empirically inaccessible features of individual muscle and tendons in biomechanical tasks. Biological neuromuscular systems are generally able to perform a specified movement task in several ways – as they have significantly more degrees of freedom than mechanical constraints. Understanding how humans resolve these redundancies to drive individual muscles and tendons in typical joint movements is of interest in the fields of biomechanics, neuroscience and prosthetics. Many experimental studies have uncovered neural, mechanical and energetic features of individual muscle and tendon function in common tasks like walking and running. However, a unifying theoretical framework that explains the many independent empirical observations is yet to be established. In this work, we show that leg muscle-tendon morphology and neural co-ordination, together, enable efficient ankle movements in walking. This finding provides quantitative insight into the operation and performance of posterior-leg muscles and tendons in walking, and motivates the idea that different muscle-tendon units take on different mechanical roles to best actuate the ankle in gait. Results reported have implications both for better understanding neuromuscular co-ordination in gait, and for the design of lower limb prosthetic and orthotic technologies. A common feature in biological neuromuscular systems is the redundancy in joint actuation. Understanding how these redundancies are resolved in typical joint movements has been a long-standing problem in biomechanics, neuroscience and prosthetics. Many empirical studies have uncovered neural, mechanical and energetic aspects of how humans resolve these degrees of freedom to actuate leg joints for common tasks like walking. However, a unifying theoretical framework that explains the many independent empirical observations and predicts individual muscle and tendon contributions to joint actuation is yet to be established. Here we develop a computational framework to address how the ankle joint actuation problem is resolved by the neuromuscular system in walking. Our framework is founded upon the proposal that a consideration of both neural control and leg muscle-tendon morphology is critical to obtain predictive, mechanistic insight into individual muscle and tendon contributions to joint actuation. We examine kinetic, kinematic and electromyographic data from healthy walking subjects to find that human leg muscle-tendon morphology and neural activations enable a metabolically optimal realization of biological ankle mechanics in walking. This optimal realization (a) corresponds to independent empirical observations of operation and performance of the soleus and gastrocnemius muscles, (b) gives rise to an efficient load-sharing amongst ankle muscle-tendon units and (c) causes soleus and gastrocnemius muscle fibers to take on distinct mechanical roles of force generation and power production at the end of stance phase in walking. The framework outlined here suggests that the dynamical interplay between leg structure and neural control may be key to the high walking economy of humans, and has implications as a means to obtain insight into empirically inaccessible features of individual muscle and tendons in biomechanical tasks. A common feature in biological neuromuscular systems is the redundancy in joint actuation. Understanding how these redundancies are resolved in typical joint movements has been a long-standing problem in biomechanics, neuroscience and prosthetics. Many empirical studies have uncovered neural, mechanical and energetic aspects of how humans resolve these degrees of freedom to actuate leg joints for common tasks like walking. However, a unifying theoretical framework that explains the many independent empirical observations and predicts individual muscle and tendon contributions to joint actuation is yet to be established. Here we develop a computational framework to address how the ankle joint actuation problem is resolved by the neuromuscular system in walking. Our framework is founded upon the proposal that a consideration of both neural control and leg muscle-tendon morphology is critical to obtain predictive, mechanistic insight into individual muscle and tendon contributions to joint actuation. We examine kinetic, kinematic and electromyographic data from healthy walking subjects to find that human leg muscle-tendon morphology and neural activations enable a metabolically optimal realization of biological ankle mechanics in walking. This optimal realization (a) corresponds to independent empirical observations of operation and performance of the soleus and gastrocnemius muscles, (b) gives rise to an efficient load-sharing amongst ankle muscle-tendon units and (c) causes soleus and gastrocnemius muscle fibers to take on distinct mechanical roles of force generation and power production at the end of stance phase in walking. The framework outlined here suggests that the dynamical interplay between leg structure and neural control may be key to the high walking economy of humans, and has implications as a means to obtain insight into empirically inaccessible features of individual muscle and tendons in biomechanical tasks. Biological neuromuscular systems are generally able to perform a specified movement task in several ways a as they have significantly more degrees of freedom than mechanical constraints. Understanding how humans resolve these redundancies to drive individual muscles and tendons in typical joint movements is of interest in the fields of biomechanics, neuroscience and prosthetics. Many experimental studies have uncovered neural, mechanical and energetic features of individual muscle and tendon function in common tasks like walking and running. However, a unifying theoretical framework that explains the many independent empirical observations is yet to be established. In this work, we show that leg muscle-tendon morphology and neural co-ordination, together, enable efficient ankle movements in walking. This finding provides quantitative insight into the operation and performance of posterior-leg muscles and tendons in walking, and motivates the idea that different muscle-tendon units take on different mechanical roles to best actuate the ankle in gait. Results reported have implications both for better understanding neuromuscular co-ordination in gait, and for the design of lower limb prosthetic and orthotic technologies. |
Audience | Academic |
Author | Krishnaswamy, Pavitra Herr, Hugh M Brown, Emery N |
AuthorAffiliation | 4 The Media Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America 3 Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, United States of America University College London, United Kingdom 2 Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America 1 Harvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America |
AuthorAffiliation_xml | – name: 3 Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, United States of America – name: 4 The Media Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – name: 2 Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – name: University College London, United Kingdom – name: 1 Harvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America |
Author_xml | – sequence: 1 givenname: Pavitra surname: Krishnaswamy fullname: Krishnaswamy, Pavitra organization: Harvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – sequence: 2 givenname: Emery N surname: Brown fullname: Brown, Emery N – sequence: 3 givenname: Hugh M surname: Herr fullname: Herr, Hugh M |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21445231$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2011 Public Library of Science Krishnaswamy et al. 2011 2011 Krishnaswamy et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Krishnaswamy P, Brown EN, Herr HM (2011) Human Leg Model Predicts Ankle Muscle-Tendon Morphology, State, Roles and Energetics in Walking. PLoS Comput Biol 7(3): e1001107. doi:10.1371/journal.pcbi.1001107 |
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Keywords | Gait Humans Computational Biology Male Musculoskeletal Physiological Phenomena Leg Ankle Walking Biomechanical Phenomena Algorithms Models, Biological Bayes Theorem Electromyography Models, Anatomic |
Language | English |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: PK. Performed the experiments: PK. Analyzed the data: PK. Wrote the paper: PK ENB HMH. Guided conception of the study, advised and oversaw the work: HMH ENB. |
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Snippet | A common feature in biological neuromuscular systems is the redundancy in joint actuation. Understanding how these redundancies are resolved in typical joint... A common feature in biological neuromuscular systems is the redundancy in joint actuation. Understanding how these redundancies are resolved in typical joint... |
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SubjectTerms | Algorithms Ankle Ankle - anatomy & histology Ankle - physiology Bayes Theorem Biomechanical Phenomena - physiology Biomechanics Biophysics/Theory and Simulation Computational Biology Computational Biology/Systems Biology Computer Science/Systems and Control Theory Electromyography Experiments Gait - physiology Humans Leg - anatomy & histology Leg - physiology Male Mathematics Measurement Models, Anatomic Models, Biological Muscular system Musculoskeletal Physiological Phenomena Neuroscience/Motor Systems Neuroscience/Theoretical Neuroscience Neurosciences Objectives Physiological aspects Prostheses Studies Tendons Torque Walking Walking - physiology |
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Title | Human leg model predicts ankle muscle-tendon morphology, state, roles and energetics in walking |
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